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The Native Sacramento Valley Red Fox ______ State of California THE RESOURCES AGENCY California Department of Fish and Game The Native Sacramento Valley Red Fox ______________________________________________________________________ Radio-collared adult male Sacramento Valley red fox, north of Capay, Yolo County, Photo taken by Ben Sacks, 3/31/2010 ______________________________________________________________________ Benjamin N. Sacks1-3, Heiko U. Wittmer4, and Mark J. Statham3 1Department of Biological Sciences California State University, Sacramento 2Department of Population Health and Reproduction University of California, Davis 3Canid Diversity and Conservation Laboratory Center for Veterinary Genetics University of California, Davis 4Department of Wildlife, Fish, and Conservation Biology University of California, Davis Contractor: University Enterprises, Inc. May 30, 2010 This report should be referenced as follows: Sacks BN, Wittmer HU, Statham MJ (2010) The Native Sacramento Valley red fox. Report to the California Department of Fish and Game, May 30, 2010, 49pp. Abstract It was recently determined that the Sacramento Valley red fox (Vulpes vulpes ssp. nov.; Sacks et al. 2010), previously considered an introduced species, is indigenous to California and phylogenetically most closely related to the state-threatened Sierra Nevada red fox (Vulpes vulpes necator). Also occurring in lowland areas of the state are introduced red foxes, which derive largely from fur farm stock exhibiting ancestry from an admixture of diverse and phylogenetically distant sources. We researched the current status of the Sacramento Valley red fox, including hybridization with introduced foxes, using noninvasive genetic sampling approaches and opportunistic collection of carcasses. Due to the apparent sparseness of red foxes, search efforts were concentrated in locations where we received credible sighting reports, following broadcast solicitations for this information from the public. Objectives were to describe the current range of the native Sacramento Valley population relative to the introduced red fox population, including hybrid zones, and to compare morphometric, life-history, and habitat affinities. Within the native population, we also investigated genetic substructure and diversity, and pathogen exposure. Results can be summarized as follows: (1) Based on genetically verified samples, we estimated the current range of the native Sacramento Valley red fox to span the Valley from Cottonwood to the Delta, west of the Sacramento River, and Chico to Sacramento, east of the Sacramento River. Hybridization with introduced red foxes was observed, primarily on the southern and southeastern margins of the range, possibly facilitated by low densities of native foxes in these areas. A tentative hybrid zone was designated where it appears most hybridization has occurred. The largest continuous span of native samples was centered on the historical range. All red foxes south of the American River and Delta and west of the Sacramento Valley (Sonoma County) were found to be nonnative. (2) Although substructure within the native population was detected, it appeared to reflect heterogeneity in red fox distribution on the landscape rather than stable barriers to gene flow. Genetic diversity, indexed by heterozygosity in 33 microsatellite loci, was relatively uniform throughout the native range (He = 0.63), which was lower than in the hybrid zone (He = 0.70) or nonnative range (He = 0.69). Thus, the native Sacramento Valley red fox appears to consist of a single population. (3) Sacramento Valley red foxes were significantly longer (total body length, tail length, ear length, hind foot length) than nonnative red foxes but the two populations had similar body masses. Native and nonnative lowland red foxes could be correctly differentiated approximately 85% of the time based on discriminant functions of body mass and total body length. Additionally, the Sacramento Valley red fox and native mountain foxes, although significantly ii different in size, exhibited similar allometric proportions, which differed from Midwestern red foxes; nonnative red foxes clustered closer to Midwestern than native red foxes. In general, the phylogenetically related Sacramento Valley red fox and mountain red foxes were lankier than other red foxes examined in this study. (4) Whelping dates were estimated from body mass and hind-foot length of pups according to previously established growth curves. Both Sacramento Valley and nonnative red foxes exhibited estimated peaks in whelping around the first of March, although variability was higher in the nonnative sample. (5) Sacramento Valley red fox den sites were disproportionately associated with grasslands and away from flooded agriculture and wetlands. These findings agree with historical observations, which indicate that red foxes were once abundant in grassland portions of the Valley that were elevated above the flood plain. Given both a 65% decline in Valley grasslands since historical times and genetic (and anecdotal) evidence that Sacramento Valley red fox experienced a population decline over the same period, it seems likely that the Sacramento Valley red fox distribution in California has been tied to the distribution of grasslands. The apparent avoidance of wetlands by native red foxes also could mark an important difference from nonnative red foxes, which commonly impact endangered ground-nesting birds in coastal wetlands. Also in contrast to nonnative red foxes, native den sites were not found in heavily urbanized areas. Finer scale studies of habitat use within home ranges and habitat-specific estimates of survival and reproduction are needed to more precisely determine critical habitat characteristics for the Sacramento Valley red fox. (6) The number of pups directly observed at den sites averaged 3.2, representing a minimum estimate of litter size. Genetic analyses identified an estimated average of 2.3 adults and 5.3 pups at den sites. These estimates are comparable to those for other red fox populations. Although we did not systematically investigate or quantify pup survival, a seemingly large number of pups was found dead considering that they were opportunistically discovered. Although most were hit by cars, many were found nowhere near roads and too long post-mortem to determine causes of death. Without quantitative estimates of pup survival, recruitment, and adult survival, the significance of observed pup mortality cannot be assessed. Future studies are needed to investigate population growth rate, along with sensitivity/elasticity of vital rates and rates of specific causes of mortality. (7) Based on serological tests and DNA tests of feces, native red foxes exhibited exposure to or active infection with several pathogens potentially causing morbidity or mortality in canids, including CDV and CPV-2. Our small serological sample size combined with apparently low sensitivity of fecal PCR surveillance iii for CPV-2 prevent us from assessing potential effects of these pathogens on the Sacramento Valley population, but future surveillance is warranted, especially in the context of cause-specific mortality studies. Disease should be considered among the list of potentially important factors affecting the population. Spatial distributions of native and nonnative red foxes, along with genetic and morphometric criteria, indicate that despite limited interbreeding where the two populations come into contact, the native Sacramento Valley red fox presently retains most of its genomic integrity. Thus, while introgression occurs and could pose a greater threat in the future, some type(s) of reproductive barrier appear(s) to be in place. Reproductive phenology, which was similar between the two populations, was ruled out as a barrier to first-generation hybridization. However, the possibility remains that reproductive timing or other traits affecting fitness could be altered in F1 individuals, potentially reducing the frequency of backcrosses. Understanding mechanisms that have thus far prevented nonnative red foxes penetrating the range of native red foxes (with or without interbreeding) could be key to assessing threats from nonnative red foxes in the future. The Sacramento Valley red fox appears to satisfy at least two criteria of a California State Species of Special Concern: (1) “is experiencing, or formerly experienced, serious (noncyclical) population declines or range retractions (not reversed) that, if continued or resumed, could qualify it for State threatened or endangered status.” and (2) “has naturally small populations exhibiting high susceptibility to risk from any factor(s), that if realized, could lead to declines that would qualify it for State threatened or endangered status.” Three areas requiring future research were identified to assess the condition of the Sacramento Valley red fox subspecies with respect to criteria for State threatened or endangered status: (1) threats posed by hybridization with nonnative red foxes, (2) habitat relationships, occupancy, and abundance, including interspecific relationships with coyotes and gray foxes, and (3) population growth rate (survival, recruitment) and cause-specific mortality. iv The Native Sacramento Valley Red Fox Benjamin N. Sacks, Heiko U. Wittmer, Mark J. Statham Table of Contents Abstract.................................................................................................................................. ii Table of Contents………………………………………………………………………………….. v Introduction ………………………………………………………………………………………..
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